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Proteoglycans, Neurogenesis and Stem Cell Differentiation

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Proteoglycans in Stem Cells

Part of the book series: Biology of Extracellular Matrix ((BEM,volume 9))

Abstract

Proteoglycans (PGs) are critical components of the cellular microenvironment localised to the cell surface or within the extracellular matrix with a wide variety of functions from early development and throughout life. They are predominantly composed of a core protein to which a number of highly sulfated glycosaminoglycan side chains are attached. PG proteins are highly variable and formed by a complex temporal, posttranslational biosynthesis that confers extensive biological diversity. These glycoproteins are critical contributors and regulators of numerous cellular processes including proliferation, stem cell plasticity and self-renewal, growth factor interaction and cell signalling as well as differentiation and lineage specification. There is great interest in how these multifaceted proteins can be used to understand complex cell and developmental biology as well as potential targets or biomarkers to prevent progression and treat a number of diseases. In combination with stem cell therapies, PGs likely provide exciting targets for a number of therapeutic applications. As these complex proteins have been shown to be involved in a number of critical developmental processes including neurogenesis, this chapter summarises PGs and their influence on neurogenesis and stem cell lineage specification and provides a summary of current models exploring their role in human neurogenesis.

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References

  • Abaskharoun M, Bellemare M, Lau E, Margolis RU (2010) Glypican-1, phosphacan/receptor protein-tyrosine phosphatase-zeta/beta and its ligand, tenascin-C, are expressed by neural stem cells and neural cells derived from embryonic stem cells. ASN Neuro 2(3):e00039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aguirre A, Rubio ME, Gallo V (2010) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467(7313):323–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akiyama T, Kamimura K, Firkus C, Takeo S, Shimmi O, Nakato H (2008) Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev Biol 313(1):408–419

    Article  CAS  PubMed  Google Scholar 

  • Alexanian AR (2010) An efficient method for generation of neural-like cells from adult human bone marrow-derived mesenchymal stem cells. Regen Med 5(6):891–900

    Article  CAS  PubMed  Google Scholar 

  • Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, Barres BA (2012) Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486(7403):410–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124(3):319–335

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41(5):683–686

    Article  CAS  PubMed  Google Scholar 

  • Araujo AP, Ribeiro ME, Ricci R, Torquato RJ, Toma L, Porcionatto MA (2010) Glial cells modulate heparan sulfate proteoglycan (HSPG) expression by neuronal precursors during early postnatal cerebellar development. Int J Dev Neurosci 28(7):611–620

    Article  CAS  PubMed  Google Scholar 

  • Avalos AM, Valdivia AD, Munoz N, Herrera-Molina R, Tapia JC, Lavandero S, Chiong M, Burridge K, Schneider P, Quest AF, Leyton L (2009) Neuronal Thy-1 induces astrocyte adhesion by engaging syndecan-4 in a cooperative interaction with alphavbeta3 integrin that activates PKCalpha and RhoA. J Cell Sci 122(Pt 19):3462–3471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balordi F, Fishell G (2007) Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons. J Neurosci 27(22):5936–5947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barateiro A, Fernandes A (2014) Temporal oligodendrocyte lineage progression: in vitro models of proliferation, differentiation and myelination. Biochim Biophys Acta 1843(9):1917–1929

    Article  CAS  PubMed  Google Scholar 

  • Barkho BZ, Song H, Aimone JB, Smrt RD, Kuwabara T, Nakashima K, Gage FH, Zhao X (2006) Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells Dev 15(3):407–421

    Article  CAS  PubMed  Google Scholar 

  • Belenkaya TY, Han C, Yan D, Opoka RJ, Khodoun M, Liu H, Lin X (2004) Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119(2):231–244

    Article  CAS  PubMed  Google Scholar 

  • Belinsky GS, Sirois CL, Rich MT, Short SM, Moore AR, Gilbert SE, Antic SD (2013) Dopamine receptors in human embryonic stem cell neurodifferentiation. Stem Cells Dev 22(10):1522–1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergles DE, Richardson WD (2015) Oligodendrocyte development and plasticity. Cold Spring Harb Perspect Biol 8(2):a020453

    Article  PubMed  Google Scholar 

  • Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MS, Steier P, Kutschera W, Johnson L, Landen M, Druid H, Spalding KL, Frisen J (2012) The age of olfactory bulb neurons in humans. Neuron 74(4):634–639

    Article  CAS  PubMed  Google Scholar 

  • Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729–777

    Article  CAS  PubMed  Google Scholar 

  • Bespalov MM, Sidorova YA, Tumova S, Ahonen-Bishopp A, Magalhaes AC, Kulesskiy E, Paveliev M, Rivera C, Rauvala H, Saarma M (2011) Heparan sulfate proteoglycan syndecan-3 is a novel receptor for GDNF, neurturin, and artemin. J Cell Biol 192(1):153–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloechlinger S, Karchewski LA, Woolf CJ (2004) Dynamic changes in glypican-1 expression in dorsal root ganglion neurons after peripheral and central axonal injury. Eur J Neurosci 19(5):1119–1132

    Article  PubMed  Google Scholar 

  • Brazelton TR, Rossi FM, Keshet GI, Blau HM (2000) From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775–1779

    Google Scholar 

  • Budday S, Steinmann P, Kuhl E (2015) Physical biology of human brain development. Front Cell Neurosci 9:257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Calvi LM, Link DC (2015) The hematopoietic stem cell niche in homeostasis and disease. Blood 126(22):2443–2451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capurro MI, Xu P, Shi W, Li F, Jia A, Filmus J (2008) Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev Cell 14(5):700–711

    Article  CAS  PubMed  Google Scholar 

  • Capurro M, Martin T, Shi W, Filmus J (2014) Glypican-3 binds to Frizzled and plays a direct role in the stimulation of canonical Wnt signaling. J Cell Sci 127(Pt 7):1565–1575

    CAS  PubMed  Google Scholar 

  • Castro-Malaspina H, Gay RE, Resnick G, Kapoor N, Meyers P, Chiarieri D, McKenzie S, Broxmeyer HE, Moore MA (1980) Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 56(2):289–301

    Article  CAS  PubMed  Google Scholar 

  • Chan WK, Howe K, Clegg JM, Guimond SE, Price DJ, Turnbull JE, Pratt T (2015) 2-O heparan sulfate sulfation by Hs2st is required for Erk/Mapk signalling activation at the mid-gestational mouse telencephalic midline. PLoS One 10(6):e0130147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen XD (2010) Extracellular matrix provides an optimal niche for the maintenance and propagation of mesenchymal stem cells. Birth Defects Res C Embryo Today 90(1):45–54

    Article  CAS  PubMed  Google Scholar 

  • Chen RH, Ding WV, McCormick F (2000) Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J Biol Chem 275(23):17894–17899

    Article  CAS  PubMed  Google Scholar 

  • Chen BY, Wang X, Wang ZY, Wang YZ, Chen LW, Luo ZJ (2013) Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/beta-catenin signaling pathway. J Neurosci Res 91(1):30–41

    CAS  PubMed  Google Scholar 

  • Choi CB, Cho YK, Prakash KV, Jee BK, Han CW, Paik YK, Kim HY, Lee KH, Chung N, Rha HK (2006) Analysis of neuron-like differentiation of human bone marrow mesenchymal stem cells. Biochem Biophys Res Commun 350(1):138–146

    Article  CAS  PubMed  Google Scholar 

  • Chojnacki A, Weiss S (2004) Isolation of a novel platelet-derived growth factor-responsive precursor from the embryonic ventral forebrain. J Neurosci 24(48):10888–10899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chojnacki A, Mak G, Weiss S (2011) PDGFRalpha expression distinguishes GFAP-expressing neural stem cells from PDGF-responsive neural precursors in the adult periventricular area. J Neurosci 31(26):9503–9512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christie KJ, Emery B, Denham M, Bujalka H, Cate HS, Turnley AM (2013) Transcriptional regulation and specification of neural stem cells. Adv Exp Med Biol 786:129–155

    Article  CAS  PubMed  Google Scholar 

  • Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F (2014) Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 82(3):545–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conget PA, Minguell JJ (1999) Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol 181(1):67–73

    Article  CAS  PubMed  Google Scholar 

  • Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3(9):e283

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Corti S, Nizzardo M, Nardini M, Donadoni C, Locatelli F, Papadimitriou D, Salani S, Del Bo R, Ghezzi S, Strazzer S, Bresolin N, Comi GP (2007) Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol 205(2):547–562

    Article  CAS  PubMed  Google Scholar 

  • Cunningham SC, Kamangar F, Kim MP, Hammoud S, Haque R, Iacobuzio-Donahue C, Ashfaq R, Kern SE, Maitra A, Heitmiller RE, Choti MA, Lillemoe KD, Cameron JL, Yeo CJ, Montgomery E, Schulick RD (2006) MKK4 status predicts survival after resection of gastric adenocarcinoma. Arch Surg 141(11):1095–1099. Discussion 1100

    Article  CAS  PubMed  Google Scholar 

  • Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315(5816):1243–1249

    Article  CAS  PubMed  Google Scholar 

  • da Silva Meirelles L, Caplan AI, Nardi NB (2008) In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26(9):2287–2299

    Article  PubMed  Google Scholar 

  • Decimo I, Bifari F, Krampera M, Fumagalli G (2012) Neural stem cell niches in health and diseases. Curr Pharm Des 18(13):1755–1783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Luca A, Cerrato V, Fuca E, Parmigiani E, Buffo A, Leto K (2016) Sonic hedgehog patterning during cerebellar development. Cell Mol Life Sci 73(2):291–303

    Article  CAS  PubMed  Google Scholar 

  • Desbordes SC, Sanson B (2003) The glypican Dally-like is required for Hedgehog signalling in the embryonic epidermis of Drosophila. Development 130(25):6245–6255

    Article  CAS  PubMed  Google Scholar 

  • Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R, Wichterle H, Henderson CE, Eggan K (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321(5893):1218–1221

    Article  CAS  PubMed  Google Scholar 

  • Dityatev A, Schachner M, Sonderegger P (2010) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat Rev Neurosci 11(11):735–746

    Article  CAS  PubMed  Google Scholar 

  • Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703–716

    Article  CAS  PubMed  Google Scholar 

  • Donato R (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33(7):637–668

    Article  CAS  PubMed  Google Scholar 

  • Dreyfuss JL, Regatieri CV, Jarrouge TR, Cavalheiro RP, Sampaio LO, Nader HB (2009) Heparan sulfate proteoglycans: structure, protein interactions and cell signaling. An Acad Bras Cienc 81(3):409–429

    Article  CAS  PubMed  Google Scholar 

  • Egea V, von Baumgarten L, Schichor C, Berninger B, Popp T, Neth P, Goldbrunner R, Kienast Y, Winkler F, Jochum M, Ries C (2011) TNF-alpha respecifies human mesenchymal stem cells to a neural fate and promotes migration toward experimental glioma. Cell Death Differ 18(5):853–863

    Article  CAS  PubMed  Google Scholar 

  • Elenius K, Jalkanen M (1994) Function of the syndecans—a family of cell surface proteoglycans. J Cell Sci 107(Pt 11):2975–2982

    Article  CAS  PubMed  Google Scholar 

  • Ellis P, Fagan BM, Magness ST, Hutton S, Taranova O, Hayashi S, McMahon A, Rao M, Pevny L (2004) SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 26(2–4):148–165

    Article  CAS  PubMed  Google Scholar 

  • Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4(11):1313–1317

    Article  CAS  PubMed  Google Scholar 

  • Esko JD, Selleck SB (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71:435–471

    Article  CAS  PubMed  Google Scholar 

  • Ethell IM, Yamaguchi Y (1999) Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J Cell Biol 144(3):575–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faissner A, Reinhard J (2015) The extracellular matrix compartment of neural stem and glial progenitor cells. Glia 63(8):1330–1349

    Article  PubMed  Google Scholar 

  • Farach-Carson MC, Carson DD (2007) Perlecan—a multifunctional extracellular proteoglycan scaffold. Glycobiology 17(9):897–905

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Castaneda A, Gaultier A (2016) Adult oligodendrocyte progenitor cells—multifaceted regulators of the CNS in health and disease. Brain Behav Immun 57:1–7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fico A, De Chevigny A, Egea J, Bosl MR, Cremer H, Maina F, Dono R (2012) Modulating Glypican4 suppresses tumorigenicity of embryonic stem cells while preserving self-renewal and pluripotency. Stem Cells 30(9):1863–1874

    Article  CAS  PubMed  Google Scholar 

  • Fietz SA, Lachmann R, Brandl H, Kircher M, Samusik N, Schroder R, Lakshmanaperumal N, Henry I, Vogt J, Riehn A, Distler W, Nitsch R, Enard W, Paabo S, Huttner WB (2012) Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc Natl Acad Sci U S A 109(29):11836–11841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filmus J, Capurro M, Rast J (2008) Glypicans. Genome Biol 9(5):224

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Flaumenhaft R, Moscatelli D, Rifkin DB (1990) Heparin and heparan sulfate increase the radius of diffusion and action of basic fibroblast growth factor. J Cell Biol 111(4):1651–1659

    Article  CAS  PubMed  Google Scholar 

  • Ford-Perriss M, Turner K, Guimond S, Apedaile A, Haubeck HD, Turnbull J, Murphy M (2003) Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development. Dev Dyn 227(2):170–184

    Article  CAS  PubMed  Google Scholar 

  • Foudah D, Redondo J, Caldara C, Carini F, Tredici G, Miloso M (2013) Human mesenchymal stem cells express neuronal markers after osteogenic and adipogenic differentiation. Cell Mol Biol Lett 18(2):163–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox LE, Shen J, Ma K, Liu Q, Shi G, Pappas GD, Qu T, Cheng J (2010) Membrane properties of neuron-like cells generated from adult human bone-marrow-derived mesenchymal stem cells. Stem Cells Dev 19(12):1831–1841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedenstein AJ, Gorskaja JF, Kulagina NN (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4(5):267–274

    CAS  PubMed  Google Scholar 

  • Fuchs E, Chen T (2013) A matter of life and death: self-renewal in stem cells. EMBO Rep 14(1):39–48

    Article  CAS  PubMed  Google Scholar 

  • Fujise M, Takeo S, Kamimura K, Matsuo T, Aigaki T, Izumi S, Nakato H (2003) Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 130(8):1515–1522

    Article  CAS  PubMed  Google Scholar 

  • Funa K, Sasahara M (2014) The roles of PDGF in development and during neurogenesis in the normal and diseased nervous system. J Neuroimmune Pharmacol 9(2):168–181

    Article  PubMed  Google Scholar 

  • Gage FH (2000) Mammalian neural stem cells. Science 287(5457):1433–1438

    Article  CAS  PubMed  Google Scholar 

  • Girós A, Morante J, Gil-Sanz C, Fairen A, Costell M (2007) Perlecan controls neurogenesis in the developing telencephalon. BMC Dev Biol 7:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonzalez AM, Buscaglia M, Ong M, Baird A (1990) Distribution of basic fibroblast growth factor in the 18-day rat fetus: localization in the basement membranes of diverse tissues. J Cell Biol 110(3):753–765

    Article  CAS  PubMed  Google Scholar 

  • Gregoire CA, Goldenstein BL, Floriddia EM, Barnabe-Heider F, Fernandes KJ (2015) Endogenous neural stem cell responses to stroke and spinal cord injury. Glia 63(8):1469–1482

    Article  PubMed  Google Scholar 

  • Greig NH, Mattson MP, Perry T, Chan SL, Giordano T, Sambamurti K, Rogers JT, Ovadia H, Lahiri DK (2004) New therapeutic strategies and drug candidates for neurodegenerative diseases: p53 and TNF-alpha inhibitors, and GLP-1 receptor agonists. Ann N Y Acad Sci 1035:290–315

    Article  CAS  PubMed  Google Scholar 

  • Guillemot F, Zimmer C (2011) From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron 71(4):574–588

    Article  CAS  PubMed  Google Scholar 

  • Guimond S, Maccarana M, Olwin BB, Lindahl U, Rapraeger AC (1993) Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J Biol Chem 268(32):23906–23914

    Article  CAS  PubMed  Google Scholar 

  • Guimond SE, Puvirajesinghe TM, Skidmore MA, Kalus I, Dierks T, Yates EA, Turnbull JE (2009) Rapid purification and high sensitivity analysis of heparan sulfate from cells and tissues: toward glycomics profiling. J Biol Chem 284(38):25714–25722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hacker U, Nybakken K, Perrimon N (2005) Heparan sulphate proteoglycans: the sweet side of development. Nat Rev Mol Cell Biol 6(7):530–541

    Article  PubMed  CAS  Google Scholar 

  • Hagihara K, Watanabe K, Chun J, Yamaguchi Y (2000) Glypican-4 is an FGF2-binding heparan sulfate proteoglycan expressed in neural precursor cells. Dev Dyn 219(3):353–367

    Article  CAS  PubMed  Google Scholar 

  • Hallenbeck JM (2002) The many faces of tumor necrosis factor in stroke. Nat Med 8(12):1363–1368

    Article  CAS  PubMed  Google Scholar 

  • Han C, Belenkaya TY, Wang B, Lin X (2004) Drosophila glypicans control the cell-to-cell movement of Hedgehog by a dynamin-independent process. Development 131(3):601–611

    Article  CAS  PubMed  Google Scholar 

  • Han C, Yan D, Belenkaya TY, Lin X (2005) Drosophila glypicans Dally and Dally-like shape the extracellular Wingless morphogen gradient in the wing disc. Development 132(4):667–679

    Article  CAS  PubMed  Google Scholar 

  • Harmer N (2006) Insights into the role of heparan sulphate in fibroblast growth factor signalling. Biochem Soc Trans 34(Pt 3):442–445

    Article  CAS  PubMed  Google Scholar 

  • Hass R, Kasper C, Bohm S, Jacobs R (2011) Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 9:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, Maisel M, Lerche H, Schwarz J, Brenner R, Storch A (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117(Pt 19):4411–4422

    Article  CAS  PubMed  Google Scholar 

  • Hermann A, Maisel M, Storch A (2006) Epigenetic conversion of human adult bone mesodermal stromal cells into neuroectodermal cell types for replacement therapy of neurodegenerative disorders. Expert Opin Biol Ther 6(7):653–670

    Article  CAS  PubMed  Google Scholar 

  • Hienola A, Tumova S, Kulesskiy E, Rauvala H (2006) N-syndecan deficiency impairs neural migration in brain. J Cell Biol 174(4):569–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homem CC, Repic M, Knoblich JA (2015) Proliferation control in neural stem and progenitor cells. Nat Rev Neurosci 16(11):647–659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howell MD, Gottschall PE (2012) Lectican proteoglycans, their cleaving metalloproteinases, and plasticity in the central nervous system extracellular microenvironment. Neuroscience 217:6–18

    Article  CAS  PubMed  Google Scholar 

  • Hsueh YP, Sheng M (1999) Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J Neurosci 19(17):7415–7425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsueh YP, Yang FC, Kharazia V, Naisbitt S, Cohen AR, Weinberg RJ, Sheng M (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 142(1):139–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang ML, Smith RA, Trieger GW, Godula K (2014) Glycocalyx remodeling with proteoglycan mimetics promotes neural specification in embryonic stem cells. J Am Chem Soc 136(30):10565–10568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubmacher D, Apte SS (2013) The biology of the extracellular matrix: novel insights. Curr Opin Rheumatol 25(1):65–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huynh MB, Ouidja MO, Chantepie S, Carpentier G, Maiza A, Zhang G, Vilares J, Raisman-Vozari R, Papy-Garcia D (2019) Glycosaminoglycans from Alzheimer’s disease hippocampus have altered capacities to bind and regulate growth factors activities and to bind tau. PLoS One 14(1):e0209573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeya M, Lee SM, Johnson JE, McMahon AP, Takada S (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389(6654):966–970

    Article  CAS  PubMed  Google Scholar 

  • Islam O, Loo TX, Heese K (2009) Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor, MAP kinase, AKT, and STAT-3 signaling pathways. Curr Neurovasc Res 6(1):42–53

    Article  CAS  PubMed  Google Scholar 

  • Itsykson P, Ilouz N, Turetsky T, Goldstein RS, Pera MF, Fishbein I, Segal M, Reubinoff BE (2005) Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol Cell Neurosci 30(1):24–36

    Article  CAS  PubMed  Google Scholar 

  • Iwata T, Hevner RF (2009) Fibroblast growth factor signaling in development of the cerebral cortex. Dev Growth Differ 51(3):299–323

    Article  CAS  PubMed  Google Scholar 

  • Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A (2006) PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51(2):187–199

    Article  CAS  PubMed  Google Scholar 

  • Jen YH, Musacchio M, Lander AD (2009) Glypican-1 controls brain size through regulation of fibroblast growth factor signaling in early neurogenesis. Neural Dev 4:33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanato Y, Ono S, Kitajima K, Sato C (2009) Complex formation of a brain-derived neurotrophic factor and glycosaminoglycans. Biosci Biotechnol Biochem 73(12):2735–2741

    Article  CAS  PubMed  Google Scholar 

  • Kaplan MS, Bell DH (1984) Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4(6):1429–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197(4308):1092–1094

    Article  CAS  PubMed  Google Scholar 

  • Kerever A, Mercier F, Nonaka R, de Vega S, Oda Y, Zalc B, Okada Y, Hattori N, Yamada Y, Arikawa-Hirasawa E (2014) Perlecan is required for FGF-2 signaling in the neural stem cell niche. Stem Cell Res 12(2):492–505

    Article  CAS  PubMed  Google Scholar 

  • Khakh BS, Sofroniew MV (2015) Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci 18(7):942–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirkpatrick CA, Dimitroff BD, Rawson JM, Selleck SB (2004) Spatial regulation of Wingless morphogen distribution and signaling by Dally-like protein. Dev Cell 7(4):513–523

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick CA, Knox SM, Staatz WD, Fox B, Lercher DM, Selleck SB (2006) The function of a Drosophila glypican does not depend entirely on heparan sulfate modification. Dev Biol 300(2):570–582

    Article  CAS  PubMed  Google Scholar 

  • Klagsbrun M (1990) The affinity of fibroblast growth factors (FGFs) for heparin; FGF-heparan sulfate interactions in cells and extracellular matrix. Curr Opin Cell Biol 2(5):857–863

    Article  CAS  PubMed  Google Scholar 

  • Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, Horvat V, Volk B, Kempermann G (2010) Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 5(1):e8809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Knox SM, Whitelock JM (2006) Perlecan: how does one molecule do so many things? Cell Mol Life Sci 63(21):2435–2445

    Article  CAS  PubMed  Google Scholar 

  • Ko JS, Pramanik G, Um JW, Shim JS, Lee D, Kim KH, Chung GY, Condomitti G, Kim HM, Kim H, de Wit J, Park KS, Tabuchi K, Ko J (2015) PTPsigma functions as a presynaptic receptor for the glypican-4/LRRTM4 complex and is essential for excitatory synaptic transmission. Proc Natl Acad Sci U S A 112(6):1874–1879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koopman G, Heider KH, Horst E, Adolf GR, van den Berg F, Ponta H, Herrlich P, Pals ST (1993) Activated human lymphocytes and aggressive non-Hodgkin’s lymphomas express a homologue of the rat metastasis-associated variant of CD44. J Exp Med 177(4):897–904

    Article  CAS  PubMed  Google Scholar 

  • Kraemer PM (1971a) Heparan sulfates of cultured cells. I. Membrane-associated and cell-sap species in Chinese hamster cells. Biochemistry 10(8):1437–1445

    Article  CAS  PubMed  Google Scholar 

  • Kraemer PM (1971b) Heparan sulfates of cultured cells. II. Acid-soluble and -precipitable species of different cell lines. Biochemistry 10(8):1445–1451

    Article  CAS  PubMed  Google Scholar 

  • Kriks S, Shim JW, Piao J, Ganat YM, Wakeman DR, Xie Z, Carrillo-Reid L, Auyeung G, Antonacci C, Buch A, Yang L, Beal MF, Surmeier DJ, Kordower JH, Tabar V, Studer L (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease. Nature 480(7378):547–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O’Brien TF, Kusakabe M, Steindler DA (1999) Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 156(2):333–344

    Article  CAS  PubMed  Google Scholar 

  • Kurosawa N, Chen GY, Kadomatsu K, Ikematsu S, Sakuma S, Muramatsu T (2001) Glypican-2 binds to midkine: the role of glypican-2 in neuronal cell adhesion and neurite outgrowth. Glycoconj J 18(6):499–507

    Article  CAS  PubMed  Google Scholar 

  • Lander AD, Selleck SB (2000) The elusive functions of proteoglycans: in vivo veritas. J Cell Biol 148(2):227–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanzoni G, Alviano F, Marchionni C, Bonsi L, Costa R, Foroni L, Roda G, Belluzzi A, Caponi A, Ricci F, Luigi Tazzari P, Pagliaro P, Rizzo R, Lanza F, Roberto Baricordi O, Pasquinelli G, Roda E, Paolo Bagnara G (2009) Isolation of stem cell populations with trophic and immunoregulatory functions from human intestinal tissues: potential for cell therapy in inflammatory bowel disease. Cytotherapy 11(8):1020–1031

    Article  CAS  PubMed  Google Scholar 

  • Lau E, Margolis RU (2010) Inhibitors of slit protein interactions with the heparan sulphate proteoglycan glypican-1: potential agents for the treatment of spinal cord injury. Clin Exp Pharmacol Physiol 37(4):417–421

    Article  CAS  PubMed  Google Scholar 

  • Lee PN, Pang K, Matus DQ, Martindale MQ (2006) A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 17(2):157–167

    Article  PubMed  CAS  Google Scholar 

  • Leonova EI, Galzitskaia OV (2013) Comparative characteristics of the structure and function for syndecan-1 from animal organisms. Mol Biol (Mosk) 47(3):505–512

    Article  CAS  Google Scholar 

  • Li T, Jiang L, Zhang X, Chen H (2009) In-vitro effects of brain-derived neurotrophic factor on neural progenitor/stem cells from rat hippocampus. Neuroreport 20(3):295–300

    Article  CAS  PubMed  Google Scholar 

  • Li F, Shi W, Capurro M, Filmus J (2011) Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J Cell Biol 192(4):691–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Xu M, Li X, Lv C, Zhang X, Yu H, Zhang M, Fu Y, Meng H, Zhou J (2015) Platelet-derived growth factor-B (PDGF-B) induced by hypoxia promotes the survival of pulmonary arterial endothelial cells through the PI3K/Akt/Stat3 pathway. Cell Physiol Biochem 35(2):441–451

    Article  CAS  PubMed  Google Scholar 

  • Li X, Wang C, Xiao J, McKeehan WL, Wang F (2016) Fibroblast growth factors, old kids on the new block. Semin Cell Dev Biol 53:155–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437(7063):1370–1375

    Article  CAS  PubMed  Google Scholar 

  • Lim DA, Alvarez-Buylla A (2016) The adult ventricular-subventricular zone (V-SVZ) and olfactory bulb (OB) neurogenesis. Cold Spring Harb Perspect Biol 8(5)

    Google Scholar 

  • Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28(3):713–726

    Article  CAS  PubMed  Google Scholar 

  • Lindner U, Kramer J, Rohwedel J, Schlenke P (2010) Mesenchymal stem or stromal cells: toward a better understanding of their biology? Transfus Med Hemother 37(2):75–83

    Article  PubMed  PubMed Central  Google Scholar 

  • Ling L, Nurcombe V, Cool SM (2009) Wnt signaling controls the fate of mesenchymal stem cells. Gene 433(1–2):1–7

    Article  CAS  PubMed  Google Scholar 

  • Litwack ED, Ivins JK, Kumbasar A, Paine-Saunders S, Stipp CS, Lander AD (1998) Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev Dyn 211(1):72–87

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Lyu Z, Yu Y, Zhao ZA, Hu S, Yuan L, Chen G, Chen H (2017) Synthetic glycopolymers for highly efficient differentiation of embryonic stem cells into neurons: lipo- or not? ACS Appl Mater Interfaces 9(13):11518–11527

    Article  CAS  PubMed  Google Scholar 

  • Lodish H, Berk A, Zipursky S, Matsudaira P, Baltimore D, Darnell J (2000) Molecular cell biology. W. H. Freeman, New York

    Google Scholar 

  • Lopez-Serrano C, Torres-Espin A, Hernandez J, Alvarez-Palomo AB, Requena J, Gasull X, Edel MJ, Navarro X (2016) Effects of the post-spinal cord injury microenvironment on the differentiation capacity of human neural stem cells derived from induced pluripotent stem cells. Cell Transplant 25(10):1833–1852

    Article  PubMed  Google Scholar 

  • Luxardi G, Galli A, Forlani S, Lawson K, Maina F, Dono R (2007) Glypicans are differentially expressed during patterning and neurogenesis of early mouse brain. Biochem Biophys Res Commun 352(1):55–60

    Article  CAS  PubMed  Google Scholar 

  • Ma DK, Kim WR, Ming GL, Song H (2009) Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann N Y Acad Sci 1170:664–673

    Article  PubMed  PubMed Central  Google Scholar 

  • Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF (1998) Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4(4):415–428

    Article  CAS  PubMed  Google Scholar 

  • Mackenzie F, Ruhrberg C (2012) Diverse roles for VEGF-A in the nervous system. Development 139(8):1371–1380

    Article  CAS  PubMed  Google Scholar 

  • Mansukhani A, Dell’Era P, Moscatelli D, Kornbluth S, Hanafusa H, Basilico C (1992) Characterization of the murine BEK fibroblast growth factor (FGF) receptor: activation by three members of the FGF family and requirement for heparin. Proc Natl Acad Sci U S A 89(8):3305–3309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto-Miyai K, Sokolowska E, Zurlinden A, Gee CE, Luscher D, Hettwer S, Wolfel J, Ladner AP, Ster J, Gerber U, Rulicke T, Kunz B, Sonderegger P (2009) Coincident pre- and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage. Cell 136(6):1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Mimura S, Kimura N, Hirata M, Tateyama D, Hayashida M, Umezawa A, Kohara A, Nikawa H, Okamoto T, Furue MK (2011) Growth factor-defined culture medium for human mesenchymal stem cells. Int J Dev Biol 55(2):181–187

    Article  CAS  PubMed  Google Scholar 

  • Minguell JJ, Erices A, Conget P (2001) Mesenchymal stem cells. Exp Biol Med (Maywood) 226(6):507–520

    Article  CAS  Google Scholar 

  • Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132(4):598–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura R, Nakamura F, Fukunaga S (2015) Diverse functions of perlecan in central nervous system cells in vitro. Anim Sci J 86(10):904–911

    Article  CAS  PubMed  Google Scholar 

  • Nizzardo M, Simone C, Falcone M, Locatelli F, Riboldi G, Comi GP, Corti S (2010) Human motor neuron generation from embryonic stem cells and induced pluripotent stem cells. Cell Mol Life Sci 67(22):3837–3847

    Article  CAS  PubMed  Google Scholar 

  • Nurcombe V, Ford MD, Wildschut JA, Bartlett PF (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 260(5104):103–106

    Article  CAS  PubMed  Google Scholar 

  • Ochi T, Nakatomi H, Ito A, Imai H, Okabe S, Saito N (2016) Temporal changes in the response of SVZ neural stem cells to intraventricular administration of growth factors. Brain Res 1636:118–129

    Article  CAS  PubMed  Google Scholar 

  • Ohkawara B, Yamamoto TS, Tada M, Ueno N (2003) Role of glypican 4 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 130(10):2129–2138

    Article  CAS  PubMed  Google Scholar 

  • Oikari LE, Griffiths LR, Haupt LM (2014) The current state of play in human neural stem cell models: what we have learnt from the rodent. OA Stem Cells 2(1):7

    Google Scholar 

  • Oikari LE, Okolicsanyi RK, Qin A, Yu C, Griffiths LR, Haupt LM (2016) Cell surface heparan sulfate proteoglycans as novel markers of human neural stem cell fate determination. Stem Cell Res 16(1):92–104

    Article  CAS  PubMed  Google Scholar 

  • Oikari LE, Yu C, Okolicsanyi RK, Avgan N, Peall IW, Griffiths LR, Haupt LM (2020) HSPGs glypican-1 and glypican-4 are human neuronal proteins characteristic of different neural phenotypes. J Neuorsci Res 98:1619–1645

    Google Scholar 

  • Ojeh N, Pastar I, Tomic-Canic M, Stojadinovic O (2015) Stem cells in skin regeneration, wound healing, and their clinical applications. Int J Mol Sci 16(10):25476–25501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 306(2):349–356

    Article  CAS  PubMed  Google Scholar 

  • Okolicsanyi RK, Griffiths LR, Haupt LM (2014) Mesenchymal stem cells, neural lineage potential, heparan sulfate proteoglycans and the matrix. Dev Biol 388(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Okolicsanyi RK, Camilleri ET, Oikari LE, Yu C, Cool SM, van Wijnen AJ, Griffiths LR, Haupt LM (2015) Human mesenchymal stem cells retain multilineage differentiation capacity including neural marker expression after extended in vitro expansion. PLoS One 10(9):e0137255

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okolicsanyi RK, Oikari LE, Yu C, Griffiths LR, Haupt LM (2018) Heparan sulfate proteoglycans as drivers of neural progenitors derived from human mesenchymal stem cells. Front Mol Neurosci 11:134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oohira A, Matsui F, Tokita Y, Yamauchi S, Aono S (2000) Molecular interactions of neural chondroitin sulfate proteoglycans in the brain development. Arch Biochem Biophys 374(1):24–34

    Article  CAS  PubMed  Google Scholar 

  • Ornitz DM, Yayon A, Flanagan JG, Svahn CM, Levi E, Leder P (1992) Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol Cell Biol 12(1):240–247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palma V, Carrasco H, Reinchisi G, Olivares G, Faunes F, Larrain J (2011) SHh activity and localization is regulated by perlecan. Biol Res 44(1):63–67

    Article  CAS  PubMed  Google Scholar 

  • Palmer TD, Ray J, Gage FH (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6(5):474–486

    Article  CAS  PubMed  Google Scholar 

  • Park D, Xiang AP, Mao FF, Zhang L, Di CG, Liu XM, Shao Y, Ma BF, Lee JH, Ha KS, Walton N, Lahn BT (2010) Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 28(12):2162–2171

    Article  CAS  PubMed  Google Scholar 

  • Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A (2012) Glial cells in (patho)physiology. J Neurochem 121(1):4–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pera MF, Andrade J, Houssami S, Reubinoff B, Trounson A, Stanley EG, Ward-van Oostwaard D, Mummery C (2004) Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J Cell Sci 117(Pt 7):1269–1280

    Article  CAS  PubMed  Google Scholar 

  • Perrimon N, Bernfield M (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404(6779):725–728

    Article  CAS  PubMed  Google Scholar 

  • Pickford CE, Holley RJ, Rushton G, Stavridis MP, Ward CM, Merry CL (2011) Specific glycosaminoglycans modulate neural specification of mouse embryonic stem cells. Stem Cells 29(4):629–640

    Article  CAS  PubMed  Google Scholar 

  • Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147

    Article  CAS  PubMed  Google Scholar 

  • Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276(5309):71–74

    Article  CAS  PubMed  Google Scholar 

  • Pucci-Minafra I, Albanese NN, Di Cara G, Minafra L, Marabeti MR, Cancemi P (2008) Breast cancer cells exhibit selective modulation induced by different collagen substrates. Connect Tissue Res 49(3):252–256

    Article  CAS  PubMed  Google Scholar 

  • Pulsipher A, Griffin ME, Stone SE, Hsieh-Wilson LC (2015) Long-lived engineering of glycans to direct stem cell fate. Angew Chem Int Ed Engl 54(5):1466–1470

    Article  CAS  PubMed  Google Scholar 

  • Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2006) Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494(3):415–434

    Article  PubMed  Google Scholar 

  • Ragni E, Vigano M, Parazzi V, Montemurro T, Montelatici E, Lavazza C, Budelli S, Vecchini A, Rebulla P, Giordano R, Lazzari L (2013) Adipogenic potential in human mesenchymal stem cells strictly depends on adult or foetal tissue harvest. Int J Biochem Cell Biol 45(11):2456–2466

    Article  CAS  PubMed  Google Scholar 

  • Rakic S, Zecevic N (2003) Early oligodendrocyte progenitor cells in the human fetal telencephalon. Glia 41(2):117–127

    Article  PubMed  Google Scholar 

  • Ramasamy S, Narayanan G, Sankaran S, Yu YH, Ahmed S (2013) Neural stem cell survival factors. Arch Biochem Biophys 534(1–2):71–87

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, Mira H, Escribano J, Farinas I (2006) Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9(3):331–339

    Article  CAS  PubMed  Google Scholar 

  • Rao MS, Hattiangady B, Shetty AK (2006) The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5(6):545–558

    Article  CAS  PubMed  Google Scholar 

  • Rapraeger A (1989) Transforming growth factor (type beta) promotes the addition of chondroitin sulfate chains to the cell surface proteoglycan (syndecan) of mouse mammary epithelia. J Cell Biol 109(5):2509–2518

    Article  CAS  PubMed  Google Scholar 

  • Reeves SA, Helman LJ, Allison A, Israel MA (1989) Molecular cloning and primary structure of human glial fibrillary acidic protein. Proc Natl Acad Sci U S A 86(13):5178–5182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhard J, Brosicke N, Theocharidis U, Faissner A (2016) The extracellular matrix niche microenvironment of neural and cancer stem cells in the brain. Int J Biochem Cell Biol 81(Pt A):174–183

    Google Scholar 

  • Reynolds BA, Rietze RL (2005) Neural stem cells and neurospheres—re-evaluating the relationship. Nat Methods 2(5):333–336

    Article  CAS  PubMed  Google Scholar 

  • Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255(5052):1707–1710

    Article  CAS  PubMed  Google Scholar 

  • Ronca F, Andersen JS, Paech V, Margolis RU (2001) Characterization of Slit protein interactions with glypican-1. J Biol Chem 276(31):29141–29147

    Article  CAS  PubMed  Google Scholar 

  • Rotter N, Oder J, Schlenke P, Lindner U, Bohrnsen F, Kramer J, Rohwedel J, Huss R, Brandau S, Wollenberg B, Lang S (2008) Isolation and characterization of adult stem cells from human salivary glands. Stem Cells Dev 17(3):509–518

    Article  CAS  PubMed  Google Scholar 

  • Rowitch DH, Kriegstein AR (2010) Developmental genetics of vertebrate glial-cell specification. Nature 468(7321):214–222

    Article  CAS  PubMed  Google Scholar 

  • Rozario T, DeSimone DW (2010) The extracellular matrix in development and morphogenesis: a dynamic view. Dev Biol 341(1):126–140

    Article  CAS  PubMed  Google Scholar 

  • Ruiz i Altaba A, Palma V, Dahmane N (2002) Hedgehog-Gli signalling and the growth of the brain. Nat Rev Neurosci 3(1):24–33

    Article  CAS  PubMed  Google Scholar 

  • Sadan O, Melamed E, Offen D (2009) Bone-marrow-derived mesenchymal stem cell therapy for neurodegenerative diseases. Expert Opin Biol Ther 9(12):1487–1497

    Article  CAS  PubMed  Google Scholar 

  • Sakane H, Yamamoto H, Matsumoto S, Sato A, Kikuchi A (2012) Localization of glypican-4 in different membrane microdomains is involved in the regulation of Wnt signaling. J Cell Sci 125(Pt 2):449–460

    Article  CAS  PubMed  Google Scholar 

  • Sakiyama-Elbert SE (2014) Incorporation of heparin into biomaterials. Acta Biomater 10(4):1581–1587

    Article  CAS  PubMed  Google Scholar 

  • Saksela O, Moscatelli D, Sommer A, Rifkin DB (1988) Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J Cell Biol 107(2):743–751

    Article  CAS  PubMed  Google Scholar 

  • Salehi Z (2009) In vivo injection of fibroblast growth factor-2 into the cisterna magna induces glypican-6 expression in mouse brain tissue. J Clin Neurosci 16(5):689–692

    Article  CAS  PubMed  Google Scholar 

  • Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427(6976):740–744

    Article  CAS  PubMed  Google Scholar 

  • Sanderson RD, Bernfield M (1988) Molecular polymorphism of a cell surface proteoglycan: distinct structures on simple and stratified epithelia. Proc Natl Acad Sci U S A 85(24):9562–9566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanderson RD, Turnbull JE, Gallagher JT, Lander AD (1994) Fine structure of heparan sulfate regulates syndecan-1 function and cell behavior. J Biol Chem 269(18):13100–13106

    Article  CAS  PubMed  Google Scholar 

  • Sarrazin S, Lamanna WC, Esko JD (2011) Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 3(7)

    Google Scholar 

  • Saunders S, Paine-Saunders S, Lander AD (1997) Expression of the cell surface proteoglycan glypican-5 is developmentally regulated in kidney, limb, and brain. Dev Biol 190(1):78–93

    Article  CAS  PubMed  Google Scholar 

  • Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A (2006) New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311(5761):629–632

    Article  CAS  PubMed  Google Scholar 

  • Schlessinger J (2000) Cell signaling by receptor tyrosine kinases. Cell 103(2):211–225

    Article  CAS  PubMed  Google Scholar 

  • Seaberg RM, van der Kooy D (2003) Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci 26(3):125–131

    Article  CAS  PubMed  Google Scholar 

  • Shigetomi E, Patel S, Khakh BS (2016) Probing the complexities of astrocyte calcium signaling. Trends Cell Biol 26(4):300–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shim AH, Liu H, Focia PJ, Chen X, Lin PC, He X (2010) Structures of a platelet-derived growth factor/propeptide complex and a platelet-derived growth factor/receptor complex. Proc Natl Acad Sci U S A 107(25):11307–11312

    Article  CAS  PubMed  Google Scholar 

  • Shimada T, Yasuda S, Sugiura H, Yamagata K (2019) Syntenin: PDZ protein regulating signaling pathways and cellular functions. Int J Mol Sci 20(17)

    Google Scholar 

  • Shin S, Mitalipova M, Noggle S, Tibbitts D, Venable A, Rao R, Stice SL (2006) Long-term proliferation of human embryonic stem cell-derived neuroepithelial cells using defined adherent culture conditions. Stem Cells 24(1):125–138

    Article  PubMed  Google Scholar 

  • Shin S, Sun Y, Liu Y, Khaner H, Svant S, Cai J, Xu QX, Davidson BP, Stice SL, Smith AK, Goldman SA, Reubinoff BE, Zhan M, Rao MS, Chesnut JD (2007) Whole genome analysis of human neural stem cells derived from embryonic stem cells and stem and progenitor cells isolated from fetal tissue. Stem Cells 25(5):1298–1306

    Article  CAS  PubMed  Google Scholar 

  • Shin JG, Kim HJ, Park BL, Bae JS, Kim LH, Cheong HS, Shin HD (2013) Putative association of GPC5 polymorphism with the risk of inflammatory demyelinating diseases. J Neurol Sci 335(1–2):82–88

    Article  CAS  PubMed  Google Scholar 

  • Silbereis JC, Pochareddy S, Zhu Y, Li M, Sestan N (2016) The cellular and molecular landscapes of the developing human central nervous system. Neuron 89(2):248–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith EM, Mitsi M, Nugent MA, Symes K (2009) PDGF-A interactions with fibronectin reveal a critical role for heparan sulfate in directed cell migration during Xenopus gastrulation. Proc Natl Acad Sci U S A 106(51):21683–21688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35

    Article  PubMed  Google Scholar 

  • Soleman S, Filippov MA, Dityatev A, Fawcett JW (2013) Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253:194–213

    Article  CAS  PubMed  Google Scholar 

  • Song HH, Shi W, Filmus J (1997) OCI-5/rat glypican-3 binds to fibroblast growth factor-2 but not to insulin-like growth factor-2. J Biol Chem 272(12):7574–7577

    Article  CAS  PubMed  Google Scholar 

  • Song HH, Shi W, Xiang YY, Filmus J (2005) The loss of glypican-3 induces alterations in Wnt signaling. J Biol Chem 280(3):2116–2125

    Article  CAS  PubMed  Google Scholar 

  • Sosunov AA, Wu X, Tsankova NM, Guilfoyle E, McKhann GM 2nd, Goldman JE (2014) Phenotypic heterogeneity and plasticity of isocortical and hippocampal astrocytes in the human brain. J Neurosci 34(6):2285–2298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisen J (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153(6):1219–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein JL, de la Torre-Ubieta L, Tian Y, Parikshak NN, Hernandez IA, Marchetto MC, Baker DK, Lu D, Hinman CR, Lowe JK, Wexler EM, Muotri AR, Gage FH, Kosik KS, Geschwind DH (2014) A quantitative framework to evaluate modeling of cortical development by neural stem cells. Neuron 83(1):69–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stipp CS, Litwack ED, Lander AD (1994) Cerebroglycan: an integral membrane heparan sulfate proteoglycan that is unique to the developing nervous system and expressed specifically during neuronal differentiation. J Cell Biol 124(1–2):149–160

    Article  CAS  PubMed  Google Scholar 

  • Suh H, Consiglio A, Ray J, Sawai T, D’Amour KA, Gage FH (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1(5):515–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Pollard S, Conti L, Toselli M, Biella G, Parkin G, Willatt L, Falk A, Cattaneo E, Smith A (2008) Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci 38(2):245–258

    Article  CAS  PubMed  Google Scholar 

  • Taipale J, Keski-Oja J (1997) Growth factors in the extracellular matrix. FASEB J 11(1):51–59

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676

    Article  CAS  PubMed  Google Scholar 

  • Tao H, Rao R, Ma DD (2005) Cytokine-induced stable neuronal differentiation of human bone marrow mesenchymal stem cells in a serum/feeder cell-free condition. Dev Growth Differ 47(6):423–433

    Article  CAS  PubMed  Google Scholar 

  • Teratani-Ota Y, Yamamizu K, Piao Y, Sharova L, Amano M, Yu H, Schlessinger D, Ko MS, Sharov AA (2016) Induction of specific neuron types by overexpression of single transcription factors. Vitro Cell Dev Biol Anim 52(9):961–973

    Article  CAS  Google Scholar 

  • Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147

    Article  CAS  PubMed  Google Scholar 

  • Tkachenko E, Rhodes JM, Simons M (2005) Syndecans: new kids on the signaling block. Circ Res 96(5):488–500

    Article  CAS  PubMed  Google Scholar 

  • Tracy ET, Zhang CY, Gentry T, Shoulars KW, Kurtzberg J (2011) Isolation and expansion of oligodendrocyte progenitor cells from cryopreserved human umbilical cord blood. Cytotherapy 13(6):722–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, van der Kooy D (2001) Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30(1):65–78

    Article  CAS  PubMed  Google Scholar 

  • Trounson A (2006) The production and directed differentiation of human embryonic stem cells. Endocr Rev 27(2):208–219

    Article  PubMed  Google Scholar 

  • Turrin NP, Rivest S (2006) Tumor necrosis factor alpha but not interleukin 1 beta mediates neuroprotection in response to acute nitric oxide excitotoxicity. J Neurosci 26(1):143–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinci L, Ravarino A, Fanos V, Naccarato AG, Senes G, Gerosa C, Bevilacqua G, Faa G, Ambu R (2016) Immunohistochemical markers of neural progenitor cells in the early embryonic human cerebral cortex. Eur J Histochem 60(1):2563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Liu F, Liu YY, Zhao CH, You Y, Wang L, Zhang J, Wei B, Ma T, Zhang Q, Zhang Y, Chen R, Song H, Yang Z (2011) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res 21(11):1534–1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Yang L, Alexander C, Temple S (2012) The niche factor syndecan-1 regulates the maintenance and proliferation of neural progenitor cells during mammalian cortical development. PLoS One 7(8):e42883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Lyu Z, Chen G, Wang H, Yuan Y, Ding K, Yu Q, Yuan L, Chen H (2015) A new avenue to the synthesis of GAG-mimicking polymers highly promoting neural differentiation of embryonic stem cells. Chem Commun (Camb) 51(84):15434–15437

    Article  CAS  Google Scholar 

  • Wang M, Liu X, Lyu Z, Gu H, Li D, Chen H (2017) Glycosaminoglycans (GAGs) and GAG mimetics regulate the behavior of stem cell differentiation. Colloids Surf B Biointerfaces 150:175–182

    Article  CAS  PubMed  Google Scholar 

  • Wegner M (2008) A matter of identity: transcriptional control in oligodendrocytes. J Mol Neurosci 35(1):3–12

    Article  CAS  PubMed  Google Scholar 

  • Wei Z, Liao J, Qi F, Meng Z, Pan S (2015) Evidence for the contribution of BDNF-TrkB signal strength in neurogenesis: an organotypic study. Neurosci Lett 606:48–52

    Article  CAS  PubMed  Google Scholar 

  • Willerth SM, Rader A, Sakiyama-Elbert SE (2008) The effect of controlled growth factor delivery on embryonic stem cell differentiation inside fibrin scaffolds. Stem Cell Res 1(3):205–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson SI, Edlund T (2001) Neural induction: toward a unifying mechanism. Nat Neurosci 4(Suppl):1161–1168

    Article  CAS  PubMed  Google Scholar 

  • Wilson NH, Stoeckli ET (2013) Sonic hedgehog regulates its own receptor on postcrossing commissural axons in a glypican1-dependent manner. Neuron 79(3):478–491

    Article  CAS  PubMed  Google Scholar 

  • Winkler S, Stahl RC, Carey DJ, Bansal R (2002) Syndecan-3 and perlecan are differentially expressed by progenitors and mature oligodendrocytes and accumulate in the extracellular matrix. J Neurosci Res 69(4):477–487

    Article  CAS  PubMed  Google Scholar 

  • Wojnacki J, Galli T (2016) Membrane traffic during axon development. Dev Neurobiol 76(11):1185–1200

    Article  PubMed  Google Scholar 

  • Xiong A, Kundu S, Forsberg-Nilsson K (2014) Heparan sulfate in the regulation of neural differentiation and glioma development. FEBS J 281(22):4993–5008

    Article  CAS  PubMed  Google Scholar 

  • Xu JC, Xiao MF, Jakovcevski I, Sivukhina E, Hargus G, Cui YF, Irintchev A, Schachner M, Bernreuther C (2014) The extracellular matrix glycoprotein tenascin-R regulates neurogenesis during development and in the adult dentate gyrus of mice. J Cell Sci 127(Pt 3):641–652

    CAS  PubMed  Google Scholar 

  • Yamaguchi Y (2001) Heparan sulfate proteoglycans in the nervous system: their diverse roles in neurogenesis, axon guidance, and synaptogenesis. Semin Cell Dev Biol 12(2):99–106

    Article  CAS  PubMed  Google Scholar 

  • Yamashita M (2013) From neuroepithelial cells to neurons: changes in the physiological properties of neuroepithelial stem cells. Arch Biochem Biophys 534(1–2):64–70

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Wang A, Feng L, Wang Y, Zhang H, Zhang I, Bany BM, Ma L (2018) Heparan sulfate proteoglycan sulfation regulates uterine differentiation and signaling during embryo implantation. Endocrinology 159(6):2459–2472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ying QL, Stavridis M, Griffiths D, Li M, Smith A (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21(2):183–186

    Article  CAS  PubMed  Google Scholar 

  • Yu P, Pearson CS, Geller HM (2018) Flexible roles for proteoglycan sulfation and receptor signaling. Trends Neurosci 41(1):47–61

    Article  CAS  PubMed  Google Scholar 

  • Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19(12):1129–1133

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Chai X, Frotscher M (2007) Balance between neurogenesis and gliogenesis in the adult hippocampus: role for reelin. Dev Neurosci 29(1–2):84–90

    Article  CAS  PubMed  Google Scholar 

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Okolicsanyi, R.K., Oikari, L.E., Yu, C., Haupt, L.M. (2021). Proteoglycans, Neurogenesis and Stem Cell Differentiation. In: Götte, M., Forsberg-Nilsson, K. (eds) Proteoglycans in Stem Cells. Biology of Extracellular Matrix, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-73453-4_6

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